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Insectivorous Birds Increase Pine but Not Parasitic Mistletoe Growth

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Insectivorous Birds Increase Pine but Not Parasitic Mistletoe Growth Journal of Animal Blackwell Publishing Ltd Ecology 2006 Contrasting cascades: insectivorous birds increase pine but 75, 350–357 not parasitic mistletoe growth KAILEN A. MOONEY* and YAN B. LINHART University of Colorado, Department Ecology and Evolutionary Biology, Boulder, CO 80309-0334, USA Summary 1. Intraguild predation occurs when top predators feed upon both intermediate predators and herbivores. Intraguild predators may thus have little net impact on her- bivore abundance. Variation among communities in the strength of trophic cascades (the indirect effects of predators on plants) may be due to differing frequencies of intraguild predation. Less is known about the influence of variation within communities in predator–predator interactions upon trophic cascade strength. 2. We compared the effects of a single predator community between two sympatric plants and two herbivore guilds. We excluded insectivorous birds with cages from ponderosa pine Pinus ponderosa trees parasitized by dwarf mistletoe Arceuthobium vaginatum. For 3 years we monitored caged and control trees for predatory arthropods that moved between the two plants, foliage-feeding caterpillars and sap-feeding hemi- pterans that were host-specific, and plant damage and growth. 3. Excluding birds increased the abundance of ant-tended aphids on pine and resulted in an 11% reduction in pine woody growth. Mutualist ants protected pine-feeding aphids from predatory arthropods, allowing aphid populations to burgeon in cages even though predatory arthropods also increased in cages. By protecting pine-feeding aphids from predatory arthropods but not birds, mutualist ants created a three-tiered linear food chain where bird effects cascaded to pine growth via aphids. 4. In contrast to the results for tended aphids on pine, bird exclusion had no net effects on untended pine herbivores, the proportion of pine foliage damaged by pine-feeding caterpillars, or the proportion of mistletoe plants damaged by mistletoe-feeding cater- pillars. These results suggest that arthropod predators, which were more abundant in cages as compared with control trees, compensated for bird predation of untended pine and mistletoe herbivores. 5. These contrasting effects of bird exclusion support food web theory: where birds were connected to pine by a linear food chain, a trophic cascade occurred. Where birds fed as intraguild predators, the reticulate food webs linking birds to pine and mistletoe resulted in no net effects on herbivores or plant biomass. Our study shows that this variation in food web structure occurred between sympatric plants and within plants between differing herbivore guilds. Key-words: bird exclusion, community ecology, effect size, food web structure, indirect effect, intraguild predation, predator exclusion, top-down, tri-trophic interaction Journal of Animal Ecology (2006) 75, 350–357 doi: 10.1111/j.1365-2656.2006.01054.x progressed to the task of determining when and where Introduction top-down control is likely to be important (Matson & The long-standing debate over whether terrestrial plants Hunter 1992; Schmitz, Hamback & Beckerman 2000; are protected from herbivores by predators has now Halaj & Wise 2001). Trophic cascade theory is predi- cated on the assumption of neatly tiered trophic levels © 2006 The Authors. Correspondence and present address: Cornell University, where organisms interact through linear food chains Journal compilation Department Ecology and Evolutionary Biology. Corson (Hairston, Smith & Slobodkin 1960; Polis & Strong © 2006 British Hall, Ithaca, NY 14853, USA. Tel.: 607 255–8050. 1996). Yet when predators prey upon both herbivores Ecological Society E-mail: [email protected] and other predators, the resultant network of direct 351 and indirect interactions causes predator effects to parasites that tap into host xylem and phloem to obtain Contrasting attenuate before herbivore abundance and plant growth water, minerals and photosynthates (Hawksworth & cascades from birds are affected (Polis & Strong 1996). Variation among Wiens 1996). communities in the commonness of intraguild preda- At Manitou, mistletoe is fed upon by three specialist tion has been proposed to be responsible, in part, for herbivores: caterpillars of Dasypyga alternosquamella variation in the strength of trophic cascades (Shurin Ragonot (Pyralidae, Lepidoptera) and Promylea et al. 2002). lunigerella glendella Dyar (Pyralidae, Lepidoptera), Considerably less attention has been given to the and the sap-feeding Neoborella tumida Knight potential for trophic structure to be variable within (Miridae, Hemiptera) (Mooney 2001; Mooney 2003). communities (but see Sipura 2002; Moon & Stiling A more diverse herbivore community feeds upon pine: 2004). Among-study variation in the impacts of pred- caterpillars (three species of Geometridae, and two ators has been attributed, at least in part, to character- from other unidentified families), leaf- and plant- istics of the herbivores and plants involved (Schmitz hoppers (Homoptera, suborder Auchenorrhyncha; et al. 2000; Halaj & Wise 2001). Furthermore, there are 36 species), and the aphid Cinara schwarzii Wilson reasons to predict within-community variability in (Aphididae, Homoptera). Cinara schwarzii is a facultative trophic cascades as a function of the specific character- mutualist with wood ants Formica spp. (Formicidae), istics of the plants and herbivores involved. Plants but the hoppers at this site are not. Mistletoe and pine influence rates of herbivore damage directly through tissues damaged by caterpillars are easily recognizable, constitutive (Fritz & Simms 1992) and induced but feeding by sap-feeders is not. Based on extensive (Karban & Baldwin 1997) resistance traits, and observations conducted with this community, we are indirectly via predators (Turlings, Tumlinson & Lewis certain that these herbivores are host-specific, and that 1990; Marquis & Whelan 1996). Likewise, herbivore no herbivore feeds upon both pine and mistletoe. characteristics such as concealed vs. exposed feeding Ninety-five per cent of bird foraging on pine and modes (e.g. Fritz 1983), sequestration of plant secondary mistletoe is performed by insectivorous chickadees compounds (e.g. Dyer & Bowers 1996) and predator Parus spp. (Paridae), nuthatches Sitta spp. (Sittidae) avoidance behaviours (Preisser, Bolnick & Benard and warblers Dendroica spp. (Parulidae) (Mooney, in 2005) influence rates of predation. press). The arthropod predator community is domin- We compared the effects of insectivorous birds ated by generalists that move freely between pine and between two sympatric plants, and between two guilds mistletoe (Mooney, in press), including ants, hunting of herbivores. For 3 years we excluded birds (top spiders and web-spinning spiders. Ladybird beetle larvae predators) from ponderosa pine Pinus ponderosa Laws. and adults (Coccinellidae), lacewings (Neuroptera, scopulorum and its angiosperm parasite the south- Chrysopidae), and some hemipterans are most com- western dwarf mistletoe Arceuthobium vaginatum (Willd.) monly associated with aphids, but also prey upon other Presl ssp. cryptopodum (Engelm.) Hawksw. & Wiens. arthropods opportunistically (Dixon 2000; Wheeler Pine and mistletoe are each fed upon by separate 2001). species of foliage-chewing and sap-feeding herbivores. These are in turn preyed upon by arthropods (interme- diate predators) that move freely between the two plants. By studying a gymnosperm and a parasitic angiosperm, In late June 1999, 32 understorey pines were selected. we sought to increase the taxonomic and ecological Each was 1–3 m tall (mean ± 1 SE: 2·6 ± 0·07), and diversity of the plants for which bird effects on plant heavily parasitized by mistletoe. Ring counts of trunks growth have been measured. By comparing the effects showed them to be 71 ± 4 years old. Sixteen trees each of this single predator community between two her- were assigned to bird exclusion (cage) and control bivore guilds and between two sympatric plants, we treatments. Cages consisted of a frame of four metal sought to test whether trophic cascades vary within this bars (1·25 cm diameter) and a polyvinyl chloride community, and to associate the differing effects of plastic tubing roof wrapped in 2·5 cm mesh monofila- birds with characteristics of the herbivores and plants ment netting (Marquis & Whelan 1994). involved. Materials and methods Visual searches were used to quantify the abundance of pine herbivores and the arthropod predators that moved between both pine and mistletoe. Mistletoe-feeding © 2006 The Authors. This work was conducted at the Manitou Experimental herbivores were small and extremely cryptic in their Journal compilation Forest in Woodland Park, Colorado, U.S.A. (39°06′N, coloration, and mistletoe morphology made them © 2006 British 105°05′W) at an elevation of 2400 m. The field site difficult to detect. Consequently, data on these arthro- Ecological Society, Journal of Animal was in a pure stand of ponderosa pine parasitized by pods were not collected. Our understanding of bird Ecology, 75, south-western dwarf mistletoe. Dwarf mistletoes effects on mistletoe herbivores is thus limited to 350–357 Arceuthobium spp. (Viscaceae) are leafless, dioecious inference from data on herbivore damage to mistletoe 352 tissues (see below). At this site, mistletoe caterpillars unopened 2002 buds. The pre-experimental internodes, K. A. Mooney & were very common (as high as 2·5 per plant in 1999: which were free of foliage, were measured
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